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Psoriasis during pregnancy: characteristics and important management recommendations

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References

  • Parisi R, Symmons DP, Griffiths CE, et al. Global epidemiology of psoriasis: a systematic review of incidence and prevalence. J Invest Dermatol 2013;133(2):377-85
  • Weatherhead S, Robson SC, Reynolds NJ. Management of psoriasis in pregnancy. BMJ 2007;334(7605):1218-20
  • Bae YS, Van Voorhees AS, Hsu S, et al. Review of treatment options for psoriasis in pregnant or lactating women: from the Medical Board of the National Psoriasis Foundation. J Am Acad Dermatol 2012;67(3):459-77
  • Raychaudhuri SP, Navare T, Gross J, et al. Clinical course of psoriasis during pregnancy. Int J Dermatol 2003;42(7):518-20
  • Murase JE, Chan KK, Garite TJ, et al. Hormonal effect on psoriasis in pregnancy and post partum. Arch Dermatol 2005;141(5):601-6
  • Boyd AS, Morris LF, Phillips CM, et al. Psoriasis and pregnancy: hormone and immune system interaction. Int J Dermatol 1996;35(3):169-72
  • Aractingi S, Briand N, Le Danff C, et al. HLA-G and NK receptor are expressed in psoriatic skin: a possible pathway for regulating infiltrating T cells? Am J Pathol 2001;159(1):71-7
  • Christophers E, Mrowietz U. The inflammatory infiltrate in psoriasis. Clin Dermatol 1995;13(2):131-5
  • Kim J, Krueger JG. The immunopathogenesis of psoriasis. Dermatol Clin 2015;33(1):13-23
  • Vogel U, Denecke B, Troyanovsky SM, et al. Transcriptional activation of psoriasis-associated cytokeratin K17 by interferon-gamma. Analysis of gamma-interferon activation sites. Eur J Biochem 1995;227(1-2):143-9
  • Yip L, McCluskey J, Sinclair R. Immunological aspects of pregnancy. Clin Dermatol 2006;24(2):84-7
  • Mowad CM, Margolis DJ, Halpern AC, et al. Hormonal influences on women with psoriasis. Cutis 1998;61(5):257-60
  • McHugh NJ, Laurent MR. The effect of pregnancy on the onset of psoriatic arthritis. Br J Rheumatol 1989;28(1):50-2
  • McNeill ME. Multiple pregnancy-induced remissions of psoriatic arthritis: case report. Am J Obstet Gynecol 1988;159(4):896-7
  • Nolten WE, Rueckert PA. Elevated free cortisol index in pregnancy: possible regulatory mechanisms. Am J Obstet Gynecol 1981;139(4):492-8
  • Lin HC, Hunnicutt JN, Moustafa FA, et al. Pharmacological treatments in pregnant women with psoriasis in the U.S.A. Br J Dermatol 2014;28(10):13306
  • Gunther C, Kecskes A, Staks T, et al. Percutaneous absorption of methylprednisolone aceponate following topical application of Advantan lotion on intact, inflamed and stripped skin of male volunteers. Skin Pharmacol Appl Skin Physiol 1998;11(1):35-42
  • Dhar S, Seth J, Parikh D. Systemic side-effects of topical corticosteroids. Indian J Dermatol 2014;59(5):460-4
  • Edwards MJ, Agho K, Attia J, et al. Case-control study of cleft lip or palate after maternal use of topical corticosteroids during pregnancy. Am J Med Genet A 2003;120A(4):459-63
  • Carmichael SL, Shaw GM, Ma C, et al. Maternal corticosteroid use and orofacial clefts. Am J Obstet Gynecol 2007;197(6):585.e581-7. discussion 683-584
  • Babalola O, Strober BE. Management of psoriasis in pregnancy. Dermatol Ther 2013;26(4):285-92
  • Murase JE, Heller MM, Butler DC. Safety of dermatologic medications in pregnancy and lactation: Part I. Pregnancy. J Am Acad Dermatol 2014;70(3):401.e401-14. quiz 415
  • Chi CC, Kirtschig G, Aberer W, et al. Evidence-based (S3) guideline on topical corticosteroids in pregnancy. Br J Dermatol 2011;165(5):943-52
  • Chi CC, Lee CW, Wojnarowska F, et al. Safety of topical corticosteroids in pregnancy. Cochrane Database Syst Rev 2009(3):CD007346
  • Czeizel AE, Rockenbauer M. Population-based case-control study of teratogenic potential of corticosteroids. Teratology 1997;56(5):335-40
  • Tremezaygues L, Reichrath J. Vitamin D analogs in the treatment of psoriasis: Where are we standing and where will we be going? Dermatoendocrinol 2011;3(3):180-6
  • Kragballe K, Beck HI, Sogaard H. Improvement of psoriasis by a topical vitamin D3 analogue (MC 903) in a double-blind study. Br J Dermatol 1988;119(2):223-30
  • Miyachi Y, Ohkawara A, Ohkido M, et al. Long-term safety and efficacy of high-concentration (20 microg/g) tacalcitol ointment in psoriasis vulgaris. Eur J Dermatol 2002;12(5):463-8
  • van de Kerkhof PC, Berth-Jones J, Griffiths CE, et al. Long-term efficacy and safety of tacalcitol ointment in patients with chronic plaque psoriasis. Br J Dermatol 2002;146(3):414-22
  • Soleymani T, Hung T, Soung J. The role of vitamin D in psoriasis: a review. Int J Dermatol 2015;20(10):12790
  • Ahn CS, Awadalla F, Huang KE, et al. Patterns of vitamin D analog use for the treatment of psoriasis. J Drugs Dermatol 2013;12(8):906-10
  • Bourke JF, Mumford R, Whittaker P, et al. The effects of topical calcipotriol on systemic calcium homeostasis in patients with chronic plaque psoriasis. J Am Acad Dermatol 1997;37(6):929-34
  • Kawaguchi M, Mitsuhashi Y, Kondo S. Iatrogenic hypercalcemia due to vitamin D3 ointment (1,24(OH)2D3) combined with thiazide diuretics in a case of psoriasis. J Dermatol 2003;30(11):801-4
  • Braun GS, Witt M, Mayer V, et al. Hypercalcemia caused by vitamin D3 analogs in psoriasis treatment. Int J Dermatol 2007;46(12):1315-17
  • Calcitriol [package insert]. Galderma Laboratories, L.P; Fort Worth, Texas: 2012
  • Suzuki T, Uchiyama H, Koike Y, et al. [Reproductive and developmental toxicity studies of calcipotriol (MC903): (1)–A fertility study in rats by subcutaneous administration]. J Toxicol Sci 1996;21(Suppl 2):389-401
  • Dovonex [package insert]. Leo Pharma, Inc., Parsippany, NJ; 2009
  • Lieben L, Stockmans I, Moermans K, et al. Maternal hypervitaminosis D reduces fetal bone mass and mineral acquisition and leads to neonatal lethality. Bone 2013;57(1):123-31
  • Remitz A, Reitamo S, Erkko P, et al. Tacrolimus ointment improves psoriasis in a microplaque assay. Br J Dermatol 1999;141(1):103-7
  • Lebwohl M, Freeman AK, Chapman MS, et al. Tacrolimus ointment is effective for facial and intertriginous psoriasis. J Am Acad Dermatol 2004;51(5):723-30
  • Liao YH, Chiu HC, Tseng YS, et al. Comparison of cutaneous tolerance and efficacy of calcitriol 3 microg g(-1) ointment and tacrolimus 0.3 mg g(-1) ointment in chronic plaque psoriasis involving facial or genitofemoral areas: a double-blind, randomized controlled trial. Br J Dermatol 2007;157(5):1005-12
  • Wang C, Lin A. Efficacy of topical calcineurin inhibitors in psoriasis. J Cutan Med Surg 2014;18(1):8-14
  • Pariser D. Topical corticosteroids and topical calcineurin inhibitors in the treatment of atopic dermatitis: focus on percutaneous absorption. Am J Ther 2009;16(3):264-73
  • Krueger GG, Eichenfield L, Goodman JJ, et al. Pharmacokinetics of tacrolimus following topical application of tacrolimus ointment in adult and pediatric patients with moderate to severe atopic dermatitis. J Drugs Dermatol 2007;6(2):185-93
  • Graham-Brown RA, Grassberger M. Pimecrolimus: a review of pre-clinical and clinical data. Int J Clin Pract 2003;57(4):319-27
  • Russell RK, Richardson N, Wilson DC. Systemic absorption with complications during topical tacrolimus treatment for orofacial Crohn disease. J Pediatr Gastroenterol Nutr 2001;32(2):207-8
  • Thomson MA, Hamburger J, Stewart DG, et al. Treatment of erosive oral lichen planus with topical tacrolimus. J Dermatolog Treat 2004;15(5):308-14
  • Pitarch G, Torrijos A, Mahiques L, et al. Systemic absorption of topical tacrolimus in Pyoderma gangrenosum. Acta Derm Venereol 2006;86(1):64-5
  • Ghislain PD, De Decker I, Lachapelle JM. Efficacy and systemic absorption of topical tacrolimus used in pyoderma gangrenosum. Br J Dermatol 2004;150(5):1052-3
  • Kainz A, Harabacz I, Cowlrick IS, et al. Review of the course and outcome of 100 pregnancies in 84 women treated with tacrolimus. Transplantation 2000;70(12):1718-21
  • Jain AB, Reyes J, Marcos A, et al. Pregnancy after liver transplantation with tacrolimus immunosuppression: a single center’s experience update at 13 years. Transplantation 2003;76(5):827-32
  • Morra P, Bartle WR, Walker SE, et al. Serum concentrations of salicylic acid following topically applied salicylate derivatives. Ann Pharmacother 1996;30(9):935-40
  • Schwarb FP, Gabard B, Rufli T, et al. Percutaneous absorption of salicylic acid in man after topical administration of three different formulations. Dermatology 1999;198(1):44-51
  • Brubacher JR, Hoffman RS. Salicylism from topical salicylates: review of the literature. J Toxicol Clin Toxicol 1996;34(4):431-6
  • Bell AJ, Duggin G. Acute methyl salicylate toxicity complicating herbal skin treatment for psoriasis. Emerg Med (Fremantle) 2002;14(2):188-90
  • Werler MM, Sheehan JE, Mitchell AA. Maternal medication use and risks of gastroschisis and small intestinal atresia. Am J Epidemiol 2002;155(1):26-31
  • Kozer E, Nikfar S, Costei A, et al. Aspirin consumption during the first trimester of pregnancy and congenital anomalies: a meta-analysis. Am J Obstet Gynecol 2002;187(6):1623-30
  • Bermas BL. Non-steroidal anti inflammatory drugs, glucocorticoids and disease modifying anti-rheumatic drugs for the management of rheumatoid arthritis before and during pregnancy. Curr Opin Rheumatol 2014;26(3):334-40
  • Torloni MR, Cordioli E, Zamith MM, et al. Reversible constriction of the fetal ductus arteriosus after maternal use of topical diclofenac and methyl salicylate. Ultrasound Obstet Gynecol 2006;27(2):227-9
  • Lam J, Polifka JE, Dohil MA. Safety of dermatologic drugs used in pregnant patients with psoriasis and other inflammatory skin diseases. J Am Acad Dermatol 2008;59(2):295-315
  • Zhu JL, Hjollund NH, Andersen AM, et al. Occupational exposure to pesticides and pregnancy outcomes in gardeners and farmers: a study within the Danish National Birth Cohort. J Occup Environ Med 2006;48(4):347-52
  • Vun YY, Jones B, Al-Mudhaffer M, et al. Generalized pustular psoriasis of pregnancy treated with narrowband UVB and topical steroids. J Am Acad Dermatol 2006;54(2 Suppl):S28-30
  • Masmoudi A, Abdelmaksoud W, Ghorbel S, et al. [Impetigo herpetiformis (two cases)]. J Gynecol Obstet Biol Reprod (Paris) 2008;37(8):804-7
  • Jang MS, Baek JW, Kang DY, et al. Successful treatment with narrowband UVB phototherapy in prurigo pigmentosa associated with pregnancy. Eur J Dermatol 2011;21(4):634-5
  • Bozdag K, Ozturk S, Ermete M. A case of recurrent impetigo herpetiformis treated with systemic corticosteroids and narrowband UVB. Cutan Ocul Toxicol 2012;31(1):67-9
  • Zeichner JA. Narrowband UV-B phototherapy for the treatment of acne vulgaris during pregnancy. Arch Dermatol 2011;147(5):537-9
  • El-Saie LT, Rabie AR, Kamel MI, et al. Effect of narrowband ultraviolet B phototherapy on serum folic acid levels in patients with psoriasis. Lasers Med Sci 2011;26(4):481-5
  • Rose RF, Batchelor RJ, Turner D, et al. Narrowband ultraviolet B phototherapy does not influence serum and red cell folate levels in patients with psoriasis. J Am Acad Dermatol 2009;61(2):259-62
  • Yentzer BA, Gustafson CJ, Feldman SR. Explicit and implicit copayments for phototherapy: examining the cost of commuting. Dermatol Online J 2013;19(6):18563
  • Sheth VM, Pandya AG. Melasma: a comprehensive update: part II. J Am Acad Dermatol 2011;65(4):699-714. quiz 715
  • Bredberg A, Lambert B. Induction of SCE by DNA cross-links in human fibroblasts exposed to 8-MOP and UVA irradiation. Mutat Res 1983;118(3):191-204
  • Stern RS, Lange R. Outcomes of pregnancies among women and partners of men with a history of exposure to methoxsalen photochemotherapy (PUVA) for the treatment of psoriasis. Arch Dermatol 1991;127(3):347-50
  • Gunnarskog JG, Kallen AJ, Lindelof BG, et al. Psoralen photochemotherapy (PUVA) and pregnancy. Arch Dermatol 1993;129(3):320-3
  • Hyoun SC, Obican SG, Scialli AR. Teratogen update: methotrexate. Birth Defects Res Part A Clin Mol Teratol 2012;94(4):187-207
  • Feldkamp M, Carey JC. Clinical teratology counseling and consultation case report: low dose methotrexate exposure in the early weeks of pregnancy. Teratology 1993;47(6):533-9
  • Donnenfeld AE, Pastuszak A, Noah JS, et al. Methotrexate exposure prior to and during pregnancy. Teratology 1994;49(2):79-81
  • Kozlowski RD, Steinbrunner JV, MacKenzie AH, et al. Outcome of first-trimester exposure to low-dose methotrexate in eight patients with rheumatic disease. Am J Med 1990;88(6):589-92
  • Menter A, Korman NJ, Elmets CA, et al. Guidelines of care for the management of psoriasis and psoriatic arthritis: section 4. Guidelines of care for the management and treatment of psoriasis with traditional systemic agents. J Am Acad Dermatol 2009;61(3):451-85
  • David M, Hodak E, Lowe NJ. Adverse effects of retinoids. Med Toxicol Adverse Drug Exp 1988;3(4):273-88
  • Brindley CJ. Overview of recent clinical pharmacokinetic studies with acitretin (Ro 10-1670, etretin). Dermatologica 1989;178(2):79-87
  • Bar Oz B, Hackman R, Einarson T, et al. Pregnancy outcome after cyclosporine therapy during pregnancy: a meta-analysis. Transplantation 2001;71(8):1051-5
  • Lamarque V, Leleu MF, Monka C, et al. Analysis of 629 pregnancy outcomes in transplant recipients treated with Sandimmun. Transplant Proc 1997;29(5):2480
  • Armenti VT, Ahlswede KM, Ahlswede BA, et al. Variables affecting birthweight and graft survival in 197 pregnancies in cyclosporine-treated female kidney transplant recipients. Transplantation 1995;59(4):476-9
  • Sgro MD, Barozzino T, Mirghani HM, et al. Pregnancy outcome post renal transplantation. Teratology 2002;65(1):5-9
  • Miniero R, Tardivo I, Curtoni ES, et al. Outcome of pregnancy after organ transplantation: a retrospective survey in Italy. Transpl Int 2005;17(11):724-9
  • Lanese DM, Conger JD. Effects of endothelin receptor antagonist on cyclosporine-induced vasoconstriction in isolated rat renal arterioles. J Clin Invest 1993;91(5):2144-9
  • Solomon CG, Greene MF. Control of hypertension in pregnancy–if some is good, is more worse? N Engl J Med 2015;372(5):475-6
  • Thomas AG, Burrows L, Knight R, et al. The effect of pregnancy on cyclosporine levels in renal allograft patients. Obstet Gynecol 1997;90(6):916-19
  • Wright S, Glover M, Baker H. Psoriasis, cyclosporine, and pregnancy. Arch Dermatol 1991;127(3):426
  • Kapoor R, Kapoor JR. Cyclosporine resolves generalized pustular psoriasis of pregnancy. Arch Dermatol 2006;142(10):1373-5
  • Edmonds EV, Morris SD, Short K, et al. Pustular psoriasis of pregnancy treated with ciclosporin and high-dose prednisolone. Clin Exp Dermatol 2005;30(6):709-10
  • Finch TM, Tan CY. Pustular psoriasis exacerbated by pregnancy and controlled by cyclosporin A. Br J Dermatol 2000;142(3):582-4
  • Raddadi AA, Baker Damanhoury Z. Cyclosporin and pregnancy. Br J Dermatol 1999;140(6):1197-8
  • Schafer P. Apremilast mechanism of action and application to psoriasis and psoriatic arthritis. Biochem Pharmacol 2012;83(12):1583-90
  • Moustafa F, Feldman SR. A review of phosphodiesterase-inhibition and the potential role for phosphodiesterase 4-inhibitors in clinical dermatology. Dermatol Online J 2014;20(5):22608
  • Otezla [package insert]. Celgene Corporation; Summit, NJ: 2014
  • Treacy G. Using an analogous monoclonal antibody to evaluate the reproductive and chronic toxicity potential for a humanized anti-TNFalpha monoclonal antibody. Hum Exp Toxicol 2000;19(4):226-8
  • Menter A, Gottlieb A, Feldman SR, et al. Guidelines of care for the management of psoriasis and psoriatic arthritis: Section 1. Overview of psoriasis and guidelines of care for the treatment of psoriasis with biologics. J Am Acad Dermatol 2008;58(5):826-50
  • Davies R, Dixon WG, Watson KD, et al. Influence of anti-TNF patient warning regarding avoidance of high risk foods on rates of listeria and salmonella infections in the UK. Ann Rheum Dis 2013;72(3):461-2
  • Mervic L. Management of moderate to severe plaque psoriasis in pregnancy and lactation in the era of biologics. Acta Dermatovenerol Alp Pannonica Adriat 2014;23(2):27-31
  • Zelinkova Z, de Haar C, de Ridder L, et al. High intra-uterine exposure to infliximab following maternal anti-TNF treatment during pregnancy. Aliment Pharmacol Ther 2011;33(9):1053-8
  • Mahadevan U, Wolf DC, Dubinsky M, et al. Placental transfer of anti-tumor necrosis factor agents in pregnant patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2013;11(3):286-92. quiz e224
  • Vasiliauskas EA, Church JA, Silverman N, et al. Case report: evidence for transplacental transfer of maternally administered infliximab to the newborn. Clin Gastroenterol Hepatol 2006;4(10):1255-8
  • Berthelsen BG, Fjeldsoe-Nielsen H, Nielsen CT, et al. Etanercept concentrations in maternal serum, umbilical cord serum, breast milk and child serum during breastfeeding. Rheumatology (Oxford) 2010;49(11):2225-7
  • Murashima A, Watanabe N, Ozawa N, et al. Etanercept during pregnancy and lactation in a patient with rheumatoid arthritis: drug levels in maternal serum, cord blood, breast milk and the infant’s serum. Ann Rheum Dis 2009;68(11):1793-4
  • Cheent K, Nolan J, Shariq S, et al. Case Report: Fatal case of disseminated BCG infection in an infant born to a mother taking infliximab for Crohn’s disease. J Crohns Colitis 2010;4(5):603-5
  • Djokanovic N, Klieger-Grossmann C, Pupco A, et al. Safety of infliximab use during pregnancy. Reprod Toxicol 2011;32(1):93-7
  • Carter JD, Valeriano J, Vasey FB. Tumor necrosis factor-alpha inhibition and VATER association: a causal relationship. J Rheumatol 2006;33(5):1014-17
  • Carter JD, Ladhani A, Ricca LR, et al. A safety assessment of tumor necrosis factor antagonists during pregnancy: a review of the Food and Drug Administration database. J Rheumatol 2009;36(3):635-41
  • Winger EE, Reed JL. Was risk properly assessed in Carter, et al’s safety assessment of tumor necrosis factor antagonists during pregnancy? J Rheumatol 2009;36(9):2122; author reply 2123
  • Rump JA, Schonborn H. [Conception and course of eight pregnancies in five women on TNF blocker etanercept treatment]. Z Rheumatol 2010;69(10):903-9
  • Diav-Citrin O, Otcheretianski-Volodarsky A, Shechtman S, et al. Pregnancy outcome following gestational exposure to TNF-alpha-inhibitors: a prospective, comparative, observational study. Reprod Toxicol 2014;43:78-84
  • Berthelot JM, De Bandt M, Goupille P, et al. Exposition to anti-TNF drugs during pregnancy: outcome of 15 cases and review of the literature. Joint Bone Spine 2009;76(1):28-34
  • Roux CH, Brocq O, Breuil V, et al. Pregnancy in rheumatology patients exposed to anti-tumour necrosis factor (TNF)-alpha therapy. Rheumatology 2007;46(4):695-8
  • Natsumi I, Matsukawa Y, Miyagawa K, et al. Successful childbearing in two women with rheumatoid arthritis and a history of miscarriage after etanercept treatment. Rheumatol Int 2013;33(9):2433-5
  • Viktil KK, Engeland A, Furu K. Outcomes after anti-rheumatic drug use before and during pregnancy: a cohort study among 150,000 pregnant women and expectant fathers. Scand J Rheumatol 2012;41(3):196-201
  • Lichtenstein GR, Feagan BG, Cohen RD, et al. Serious infections and mortality in association with therapies for Crohn’s disease: TREAT registry. Clin Gastroenterol Hepatol 2006;4(5):621-30
  • Vesga L, Terdiman JP, Mahadevan U. Adalimumab use in pregnancy. Gut 2005;54(6):890
  • Schnitzler F, Fidder H, Ferrante M, et al. Outcome of pregnancy in women with inflammatory bowel disease treated with antitumor necrosis factor therapy. Inflamm Bowel Dis 2011;17(9):1846-54
  • Mahadevan U, Cucchiara S, Hyams JS, et al. The London Position Statement of the World Congress of Gastroenterology on Biological Therapy for IBD with the European Crohn’s and Colitis Organisation: pregnancy and pediatrics. Am J Gastroenterol 2011;106(2):214-23. quiz 224
  • Mishkin DS, Van Deinse W, Becker JM, et al. Successful use of adalimumab (Humira) for Crohn’s disease in pregnancy. Inflamm Bowel Dis 2006;12(8):827-8
  • Coburn LA, Wise PE, Schwartz DA. The successful use of adalimumab to treat active Crohn’s disease of an ileoanal pouch during pregnancy. Dig Dis Sci 2006;51(11):2045-7
  • Hyrich KL, Symmons DP, Watson KD, et al. Pregnancy outcome in women who were exposed to anti-tumor necrosis factor agents: results from a national population register. Arthritis Rheum 2006;54(8):2701-2
  • Martin PL, Sachs C, Imai N, et al. Development in the cynomolgus macaque following administration of ustekinumab, a human anti-IL-12/23p40 monoclonal antibody, during pregnancy and lactation. Birth Defects Res B Dev Reprod Toxicol 2010;89(5):351-63
  • Andrulonis R, Ferris LK. Treatment of severe psoriasis with ustekinumab during pregnancy. J Drugs Dermatol 2012;11(10):1240
  • Alsenaid A, Prinz JC. Inadvertent pregnancy during ustekinumab therapy in a patient with plaque psoriasis and impetigo herpetiformis. J Eur Acad Dermatol Venereol 2014;21(10):12872
  • Fotiadou C, Lazaridou E, Sotiriou E, et al. Spontaneous abortion during ustekinumab therapy. J Dermatol Case Rep 2012;6(4):105-7
  • Langley RG, Elewski BE, Lebwohl M, et al. Secukinumab in plaque psoriasis–results of two phase 3 trials. N Engl J Med 2014;371(4):326-38
  • Cosentyx [package insert]. Novartis Pharmaceuticals Corporation; East Hanover, NJ: 2015
  • Content and format of labeling for human prescription drug and biological products; requirements for pregnancy and lactation labeling. Food and Drug Administration, 2008

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